Risk of extinction of a unique skate population due to predation by a recovering marine mammal.

Benefitting from reduced harvesting and an end to culling, many marine mammals are now recovering from past overexploitation. These recoveries represent important conservation successes but present a serious conservation problem when the recovering mammals are predators of species of conservation concern. Here, we examine the role of predation by recovering grey seals (Halichoerus grypus) in the near-extinction of a unique skate population in the southern Gulf of St. Lawrence (sGSL) in Atlantic Canada. Winter skate (Leucoraja ocellata) in the sGSL are distinct from winter skate elsewhere and may represent an endemic species. Their adult abundance has declined by 98% since 1980, and these skates are now detectable in only a small fraction of their former range. Population modeling indicates that the ongoing collapse of this population is due to increases in the natural mortality of adults. Based on model projections, this population would be extinct by mid-century if its current rate of productivity were to persist. A second population model incorporated predation by grey seals. Model estimates of skate consumption by seals were consistent with historical and recent estimates of the contribution of skates to grey seal diets. The estimated consumption accounted for the increases in the natural mortality of adult skates. A Type III functional response for grey seals preying on winter skate emerged from the model results. This indicates that, when skate abundance is very low, grey seals are expected to switch to alternate prey, resulting in declines in the mortality of skates due to predation. Consequently, contrary to projections at current productivity, winter skate are expected to be trapped at very low abundance in a "predator pit" instead of declining to extinction. Nonetheless, extinction risk would remain very high at the very small population size in the predator pit. Our results emphasize the need for an ecosystem-based approach to the management of living resources in this ecosystem.

Estimating partial regulation in spatiotemporal models of community dynamics.

Niche-based approaches to community analysis often involve estimating a matrix of pairwise interactions among species (the "community matrix"), but this task becomes infeasible using observational data as the number of modeled species increases. As an alternative, neutral theories achieve parsimony by assuming that species within a trophic level are exchangeable, but generally cannot incorporate stabilizing interactions even when they are evident in field data. Finally, both regulated (niche) and unregulated (neutral) approaches have rarely been fitted directly to survey data using spatiotemporal statistical methods. We therefore propose a spatiotemporal and model-based approach to estimate community dynamics that are partially regulated. Specifically, we start with a neutral spatiotemporal model where all species follow ecological drift, which precludes estimating pairwise interactions. We then add regulatory relations until model selection favors stopping, where the "rank" of the interaction matrix may range from zero to the number of species. A simulation experiment shows that model selection can accurately identify the rank of the interaction matrix, and that the identified spatiotemporal model can estimate the magnitude of species interactions. A 40-yr case study for the Gulf of St. Lawrence marine community shows that recovering grey seals have an unregulated and negative relationship with demersal fishes. We therefore conclude that partial regulation is a plausible approximation to community dynamics using field data and hypothesize that estimating partial regulation will be expedient in future analyses of spatiotemporal community dynamics given limited field data. We conclude by recommending ongoing research to add explicit models for movement, so that meta-community theory can be confronted with data in a spatiotemporal statistical framework.

Comment on "Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery".

Pershing et al (Science, 13 November 2015, p. 809) concluded that recent warming in the Gulf of Maine contributed to the collapse of Gulf of Maine cod. We argue that this conclusion is based on a flawed analysis of the population dynamics of this cod stock. We believe that understanding the potential role of climate change in the collapse of this stock requires more defensible analyses.

Spatial distribution of fishes in a Northwest Atlantic ecosystem in relation to risk of predation by a marine mammal.

1. Numerous studies have shown that, at spatial scales of metres to several kilometres, animals balance the trade-off between foraging success and predation mortality by increasing their use of safer but less profitable habitats as predation risk increases. However, it is less clear whether prey respond similarly at the larger spatiotemporal scales of many ecosystems. 2. We determine whether this behaviour is evident in a large marine ecosystem, the southern Gulf of St. Lawrence (sGSL, 75 000 km(2) ) over a 42-year period. This ecosystem is characterized by a recent increase in the abundance of a large marine predator, the grey seal (Halichoerus grypus Fabricius), by more than an order of magnitude. 3. We compared changes in spatial distribution over the 1971-2012 period between important prey of grey seals (Atlantic cod, Gadus morhua L.; white hake, Urophycis tenuis Mitchill; and thorny skate, Amblyraja radiata Donovan) and non-prey fishes. 4. Distribution was modelled using generalized additive models incorporating spatially variable effects of predation risk, density dependence and water temperature. Distributions of cod, hake and skate were strongly related to risk of predation by seals, with distribution shifting into lower risk areas as predation risk increased. Non-prey species did not show similar changes in habitat use. Spatial variation in fish condition suggests that these low-risk areas are also less profitable for cod and skate in terms of food availability. The effects of density dependence and water temperature were also important in models, but did not account for the changes in habitat use as the risk of predation increased. 5. These results indicate that these fish are able to assess and respond to spatial variation in predation risk at very large spatial scales. They also suggest that non-consumptive 'risk' effects may be an important component of the declines in productivity of seal prey in this ecosystem, and of the indirect effects at lower trophic levels.

Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod.

Little is known about how quickly natural populations adapt to changes in their environment and how temporal and spatial variation in selection pressures interact to shape patterns of genetic diversity. We here address these issues with a series of genome scans in four overfished populations of Atlantic cod (Gadus morhua) studied over an 80-year period. Screening of >1000 gene-associated single-nucleotide polymorphisms (SNPs) identified 77 loci that showed highly elevated levels of differentiation, likely as an effect of directional selection, in either time, space or both. Exploratory analysis suggested that temporal allele frequency shifts at certain loci may correlate with local temperature variation and with life history changes suggested to be fisheries induced. Interestingly, however, largely nonoverlapping sets of loci were temporal outliers in the different populations and outliers from the 1928 to 1960 period showed almost complete stability during later decades. The contrasting microevolutionary trajectories among populations resulted in sequential shifts in spatial outliers, with no locus maintaining elevated spatial differentiation throughout the study period. Simulations of migration coupled with observations of temporally stable spatial structure at neutral loci suggest that population replacement or gene flow alone could not explain all the observed allele frequency variation. Thus, the genetic changes are likely to at least partly be driven by highly dynamic temporally and spatially varying selection. These findings have important implications for our understanding of local adaptation and evolutionary potential in high gene flow organisms and underscore the need to carefully consider all dimensions of biocomplexity for evolutionarily sustainable management.

Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua).

Fisheries-induced evolution has been hypothesized to delay the recovery of collapsed fish stocks through effects on their productivity. The cod stock in the southern Gulf of St. Lawrence (SGSL) collapsed in the early 1990s and has shown no recovery since then, due mainly to high natural mortality of adult cod. Age and size at maturation of SGSL cod decreased sharply over time in cohorts produced in the 1950s and 1960s, likely reflecting an evolutionary response to intensified fishing, and have remained low since then, despite severe reductions in fishing mortality over the past 15 years. A predicted consequence of early maturation is increased natural mortality due to higher costs to reproduction. Early maturation may be a cause of increases in natural mortality of SGSL cod in the 1970s but does not appear to be related to the much larger increases since then. Instead, the current high natural mortality of SGSL cod appears to be primarily a cause, rather than a consequence, of the continued early maturation in this population, now replacing fishing mortality as the agent of selection favouring early maturity. This striking example of the failure to reverse fisheries-induced evolution by relaxing fishing pressure emphasizes the need for management strategies that minimize the chances of harvest-induced genetic change.

Assessing threats to species at risk using stage-structured state-space models: mortality trends in skate populations.

Population models are needed to assess the threats to species at risk and to evaluate alternative management actions. Data to support modeling is limited for many species at risk, and commonly used approaches generally assume stationary vital rates, a questionable assumption given widespread ecosystem change. We describe a modeling approach that can be applied to time series of length composition data to estimate vital rates and test for changes in these rates. Our approach uses stage-structured population models fit within a Bayesian state-space model. This approach simultaneously allows for both process and observation uncertainty, and it facilitates incorporating prior information on population dynamics and on the monitoring process. We apply these models to populations of winter skate (Leucoraja ocellata) that have been designated as "endangered" or "threatened." These models indicate that natural mortality has decreased for juveniles and increased for adults in these populations. The declines observed in these populations had been attributed to unsustainable rates of bycatch in fisheries for other groundfishes; our analyses indicate that increased natural mortality of adults is also an important factor contributing to these declines. Adult natural mortality was positively related to grey seal (Halichoerus grypus) abundance, suggesting the hypothesis that increased adult mortality reflected increased predation by expanding grey seal herds. Population projections indicated that the threatened population would be expected to stabilize at a low level of abundance if all fishery removals were eliminated, but that the endangered population would likely continue to decline even in the absence of fishery removals. We note that time series of size distributions are available for most marine fish populations monitored by research surveys, and we suggest that a similar approach could be used to extract information from these time series in order to estimate mortality rates and changes in these rates.

Genetic variation in life-history reaction norms in a marine fish.

Neither the scale of adaptive variation nor the genetic basis for differential population responses to the environment is known for broadcast-spawning marine fishes. Using a common-garden experimental protocol, we document how larval growth, survival and their norms of reaction differ genetically among four populations of Atlantic cod (Gadus morhua). These traits, and their plastic responses to food and temperature, differed across spatial scales at which microsatellite DNA failed to detect population structure. Divergent survival reaction norms indicate that warm-water populations are more sensitive to changes in food, whereas cold-water populations are more sensitive to changes in temperature. Our results suggest that neither the direction nor the magnitude of demographic responses to environmental change need be the same among populations. Adaptive phenotypic plasticity, previously undocumented in marine fishes, can significantly influence the probability of recovery and persistence of collapsed populations by affecting their ability to respond to natural and anthropogenic environmental change.

Evolutionary response to size-selective mortality in an exploited fish population.

Many collapsed fish populations have failed to recover after a decade or more with little fishing. This may reflect evolutionary change in response to the highly selective mortality imposed by fisheries. Recent experimental work has demonstrated a rapid genetic change in growth rate in response to size-selective harvesting of laboratory fish populations. Here, we use a 30-year time-series of back-calculated lengths-at-age to test for a genetic response to size-selective mortality in the wild in a heavily exploited population of Atlantic cod (Gadus morhua). Controlling for the effects of density- and temperature-dependent growth, the change in mean length of 4-year-old cod between offspring and their parental cohorts was positively correlated with the estimated selection differential experienced by the parental cohorts between this age and spawning. This result supports the hypothesis that there have been genetic changes in growth in this population in response to size-selective fishing. Such changes may account for the continued small size-at-age in this population despite good conditions for growth and little fishing for over a decade. This study highlights the need for management regimes that take into account the evolutionary consequences of fishing.

Countergradient variation in body shape between two populations of Atlantic cod (Gadus morhua).

Variation in morphological traits is generally thought to be cogradient, with environmental effects on phenotypic expression reinforcing genetic differences between populations. We compared body shape between two populations of Atlantic cod (Gadus morhua). Striking shape differences occurred between juveniles from the two populations when reared in a common laboratory environment. However, no difference in body shape occurred between wild-reared juveniles from the two populations, suggesting that the genetic differences between populations were obscured by opposing effects of the environmental differences experienced in the wild. We suggest that much of the genetic diversity in body shape of fishes may be cryptic, with stabilizing selection for the same optimal phenotype resulting in genetic divergence between populations subject to contrasting environmental influences.

THE FUNCTIONAL BASIS OF NATURAL SELECTION FOR VERTEBRAL TRAITS OF LARVAE IN THE STICKLEBACK GASTEROSTEUS ACULEATUS.

Previous studies have demonstrated selective predation for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. I tested the hypothesis that this selection results from a direct functional advantage to particular vertebral phenotypes by direct measurement of the burst swimming performance of larvae. Within a narrow window of lengths, burst speed did depend on vertebral phenotype. As in the previous predation experiments, performance was related more directly to the ratio of abdominal to caudal vertebrae (VR) than to the total number of vertebrae (VN), and the optimal VR decreased as larval length increased. Changes with length in the vertebral phenotype frequencies of wild larvae provided evidence of selection for VR and for VN in the wild. Larvae with particular VR increased in frequency in the wild at just those lengths when their relative performance was superior in the laboratory. The observed pattern of length-dependent selection for vertebral number provides an explanation for the widespread trends in vertebral number that occur among populations of related fishes.

SELECTIVE PREDATION FOR VERTEBRAL PHENOTYPE IN GASTEROSTEUS ACULEATUS: REVERSAL IN THE DIRECTION OF SELECTION AT DIFFERENT LARVAL SIZES.

Variation in the number of vertebrae is widespread in fishes, and is partly genetic in origin. The adaptive significance of this variation was tested by exposing larvae of the threespine stickleback (Gasterosteus aculeatus) to predation by sunfish (Lepomis gibbosus). Two vertebral characters were considered: the total number (VN) and the ratio of abdominal to caudal vertebrae (VR). Predation was selective for both characters, but selection was more directly related to VR than to VN. The direction of selection depended on larval length: as length increased, optimal VR decreased. Total selection for VR was a combination of direct selection and an indirect effect of selection acting on a correlated trait, the ratio of precaudal to caudal length. Direct and indirect selection were in opposing directions at a given larval length. Variation in vertebral number may be maintained in populations partly because the strength of selection is reduced by opposing directions between direct and indirect selection, and between total selection at different larval lengths.